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An eye-tracker controlled cognitive battery: overcoming verbal-motor limitations in ALS

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Abstract

We assessed language, attention, executive, and social cognition abilities in a sample of patients with Amyotrophic Lateral Sclerosis (ALS) by means of a recently developed cognitive battery based on oculomotor control with eye-tracking (ET) technology. Twenty-one ALS patients and 21 age- and education-matched healthy subjects underwent the ET-based cognitive assessment, together with the standard cognitive screening tools [Frontal Assessment Battery (FAB); Montreal Cognitive Assessment (MoCA); and Digit Sequencing Task]. Psychological measures of anxiety (State-Trait Anxiety Inventory-Y) and depression (Beck Depression Inventory) were also collected, and an ET usability questionnaire was administered. For patients, clinical and respiratory examinations were also performed, together with behavioural assessment (Frontal Behavioural Inventory). The developed battery discriminated among patients and controls with regard to measures of verbal fluency, frontal abilities, and social cognition. Measures of diagnostic utility confirmed a higher diagnostic accuracy of such ET-based tests with respect to FAB; similar diagnostic accuracy emerged when comparing them to the other standard cognitive tools (MoCA, WM). Usability ratings about the ET tests were comparable among the two groups. The ET-based neuropsychological battery demonstrated good levels of diagnostic accuracy and usability in a clinical population of non-demented ALS patients, compared to matched healthy controls. Future studies will be aimed at further investigate validity and usability components by recruiting larger sample of patients, both in moderate-to-severe stages of the disease and affected by more severe cognitive impairment.

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References

  1. Phukan J, Elamin M, Bede P et al (2012) The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study. J Neurol Neurosurg Psychiatry 83(1):102–108. doi:10.1136/jnnp-2011-300188

    Article  PubMed  Google Scholar 

  2. Strong MJ, Grace GM, Freedman M et al (2009) Consensus criteria for the diagnosis of frontotemporal cognitive and behavioral syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 10:131–146. doi:10.1080/17482960802654364

    Article  PubMed  Google Scholar 

  3. Beeldman E, Raaphorst J, Klein Twennaar M et al (2015) The cognitive profile of ALS: a systematic review and meta-analysis update. J Neurol Neurosurg Psychiatry. doi:10.1136/jnnp--310734

    PubMed  Google Scholar 

  4. Consonni M, Catricalà E, Dalla Bella E et al (2016) Beyond the consensus criteria: multiple cognitive profiles in amyotrophic lateral sclerosis? Cortex 81:162–167. doi:10.1016/j.cortex.2016.04.014

    Article  PubMed  Google Scholar 

  5. Goldstein LH, Abrahams S (2013) Changes in cognition and behaviour in amyotrophic lateral sclerosis: nature of impairment and implications for assessment. Lancet Neurol 12:368–380. doi:10.1016/S1474-4422(13)70026-7

    Article  PubMed  Google Scholar 

  6. Abrahams S, Newton J, Niven E et al (2014) Screening for cognition and behaviour changes in ALS. Amyotroph Lateral Scler Frontotemporal Degener 15:9–14. doi:10.3109/21678421.2013.805784

    Article  PubMed  Google Scholar 

  7. Poletti B, Solca F, Carelli L et al (2016) The validation of the Italian Edinburgh Cognitive and Behavioural ALS Screen (ECAS). Amyotroph Lateral Scler Frontotemporal Degener 24:1–10. doi:10.1080/21678421.2016.1183679

    Google Scholar 

  8. Lulé D, Burkhardt C, Abdulla S et al (2015) The Edinburgh Cognitive and Behavioural Amyotrophic Lateral Sclerosis Screen: a cross-sectional comparison of established screening tools in a German–Swiss population. Amyotroph Lateral Scler Frontotemporal Degener 16(1–2):16–23. doi:10.3109/21678421.2014.959451

    Article  PubMed  Google Scholar 

  9. Ye S, Ji Y, Li C, He J, Liu X, Fan D (2016) The Edinburgh Cognitive and Behavioural ALS Screen in a Chinese Amyotrophic Lateral Sclerosis Population. PLoS One 11(5):155496. doi:10.1371/journal.pone.0155496

    Google Scholar 

  10. Hicks SL, Sharma R, Khan AN et al (2013) An eye-tracking version of the trail-making test. PLoS One 8(12):e84061. doi:10.1371/journal.pone.0084061

    Article  PubMed  PubMed Central  Google Scholar 

  11. Proudfoot M, Menke RAL, Sharma R et al (2015) Eye-tracking in amyotrophic lateral sclerosis: a longitudinal study of saccadic and cognitive tasks. Amyotroph Lateral Sclerosis Frontotemporal Degener 17(1–2):101–111. doi:10.3109/21678421.2015.1054292

    Google Scholar 

  12. Keller J, Gorges M, Horn HT et al (2015) Eye-tracking controlled cognitive function tests in patients with amyotrophic lateral sclerosis: a controlled proof-of-principle study. J Neurol 262:1918–1926. doi:10.1007/s00415-015-7795-3

    Article  CAS  PubMed  Google Scholar 

  13. Iversen IH, Ghanayim N, Kübler A, Neumann N, Birbaumer N, Kaiser J (2008) A brain-computer interface tool to assess cognitive functions in completely paralyzed patients with amyotrophic lateral sclerosis. Clin Neurophysiol 119:2214–2223. doi:10.1016/j.clinph.2008.07.001

    Article  CAS  PubMed  Google Scholar 

  14. Perego P, Turconi AC, Andreoni G et al (2011) Cognitive ability assessment by brain-computer interface validation of a new assessment method for cognitive abilities. J Neurosci Methods 201:239–250. doi:10.1016/j.jneumeth.2011.06.025

    Article  CAS  PubMed  Google Scholar 

  15. Keller J, Gorges M, Aho-Özhan HE et al (2016) Eye-tracking control to assess cognitive functions in patients with amyotrophic lateral sclerosis. J Vis Exp. doi:10.3791/54634

    Google Scholar 

  16. Cipresso P, Carelli L, Solca F et al (2012) The use of P300-based BCIs in amyotrophic lateral sclerosis: from augmentative and alternative communication to cognitive assessment. Brain Behav 2(4):479–498. doi:10.1002/brb3.57

    Article  PubMed  PubMed Central  Google Scholar 

  17. Cipresso P, Meriggi P, Carelli L et al (2013) Cognitive assessment of executive functions using brain computer interface and eye-tracking. EAI Endors Trans Ambient Syst 4:e4. doi:10.4108/trans.amsys.01-06.2013.e4

    Article  Google Scholar 

  18. Poletti B, Carelli L, Solca F et al (2016) Cognitive assessment in amyotrophic lateral sclerosis by means of P300-Brain Computer Interface: a preliminary study. Amyotroph Lateral Scler Frontotemporal Degener 17(7–8):473–481. doi:10.1080/21678421.2016.1181182

    Article  Google Scholar 

  19. Poletti B, Carelli L, Solca F et al (2017) An eye-tracking controlled neuropsychological battery for cognitive assessment in neurological diseases. Neurol Sci. doi:10.1007/s10072-016-2807-3

    PubMed  Google Scholar 

  20. Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of neurology Research Group on Motor Neuron Disease (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293–299. doi:10.1080/146608200300079536

    Article  CAS  PubMed  Google Scholar 

  21. Cedarbaum JM, Stambler N, Malta E et al (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessment of respiratory function. J Neurol Sci 169:13–21. doi:10.1016/S0022-510X(99)00210-5

    Article  CAS  PubMed  Google Scholar 

  22. Dubois B, Slachevsky A, Litvan I, Pillon B (2000) The FAB. A frontal assessment battery at bedside. Neurology 55:1621–1626. doi:10.1212/WNL.55.11.1621

    Article  CAS  PubMed  Google Scholar 

  23. Pirani A, Nasreddine ZS, Tulipani C, Neri M (2007) Montreal Cognitive Assessment (MOCA): uno strumento rapido per lo screening del Mild Cognitive Impairment. Dati preliminari della versione italiana. Atti IV Congresso Regionale Associazione Italiana Psicogeriatria, Bologna

  24. D’Esposito M, Postle BR (2015) The cognitive neuroscience of working memory. Annu Rev Psychol 3(66):115–142. doi:10.1146/annurev-psych-010814-015031

    Article  Google Scholar 

  25. Anselmetti S, Poletti S, Ermoli E et al (2008) The Brief Assessment of Cognition in Schizophrenia. Normative data for the Italian population. Neurol Sci 29(2):85–92. doi:10.1007/s10072-008-0866-9

    Article  PubMed  Google Scholar 

  26. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571

    Article  CAS  PubMed  Google Scholar 

  27. Spielberger CD, Gorsuch RL, Lushene R (2007) The State Trait Anxiety Inventory (STAI). Test Manual for Form X. Consulting Psychologist Press, Palo Alto (trad. Italiana a cura di Lazzari R. E Pancheri P., “S.T.A.I. Questionario di autovalutazione dell’ansia di stato e di tratto”. Organizzazioni Speciali, Firenze,1980)

  28. Alberici A, Geroldi C, Cotelli M (2007) The Frontal Behavioural Inventory (Italian version) differentiates frontotemporal lobar degeneration variants from Alzheimer’s disease. Neurol Sci 28:80–86

    Article  CAS  PubMed  Google Scholar 

  29. Novelli G, Papagno C, Capitani E, Laiacona N, Vallar G, Cappa SF (1986) Tre test clinici di ricerca e produzione lessicale. Taratura su soggetti normali. Archivio di Psicol Neurol e Psichiatria 47(4):477–506

    Google Scholar 

  30. De Renzi E, Vignolo LA (1962) The Token Test: a sensitive test to detect receptive disturbances in aphasics. Brain 85:556–678. doi:10.1093/brain/85.4.665

    Article  Google Scholar 

  31. Brickenkamp R, Zillmer E (1998) The d2 test of attention, 1st edn. Hogrefe & Huber Publishers, Seattle, WA

    Google Scholar 

  32. Raven JC (1948) The comparative assessment of intellectual ability. Br J Psychol 39:12–19. doi:10.1111/j.2044-8295.1948.tb00198.x

    Google Scholar 

  33. Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A (2004) Modified card sorting test: normative data. J Clin Exp Neuropsychol 26(2):246–250

    Article  PubMed  Google Scholar 

  34. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I (2001) The ‘‘Reading the Mind in the Eyes’’ test revised version: a study with normal adults, and adults with asperger syndrome or high-functioning autism. J Child Psychol Psychiat 42(2):241–251. doi:10.1111/1469-7610.00715

    Article  CAS  PubMed  Google Scholar 

  35. Bechara A, Tranel D, Damasio H (2000) Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain 123(pt 11):2189–2202. doi:10.1093/brain/123.11.2189

    Article  PubMed  Google Scholar 

  36. Stansfield RB, Preston S, Bechara A (2003) Normative gambling task data: Analysis summary. Normative gambling task data: Analysis summary. University of Iowa, Iowa

    Google Scholar 

  37. Youden WJ (1950) Index for rating diagnostic tests. Cancer 3:32–35

    Article  CAS  PubMed  Google Scholar 

  38. Strong MJ, Abrahams S, Goldstein LH et al (2017) Amyotrophic lateral sclerosis—frontotemporal spectrum disorder (ALS-FTSD): revised diagnostic criteria. Amyotroph Lateral Scler Frontotemporal Degener 5:1–22. doi:10.1080/21678421.2016.1267768

    Google Scholar 

  39. Phukan J, Pender NP, Hardiman O (2007) Cognitive impairment in amyotrophic lateral sclerosis. Lancet Neurol 6(11):994–1003

    Article  CAS  PubMed  Google Scholar 

  40. Sedda A (2014) Disorders of emotional processing in amyotrophic lateral sclerosis. Curr Opin Neurol 27:659–665. doi:10.1097/WCO.0000000000000147

    Article  PubMed  Google Scholar 

  41. Bora E (2017) Meta-analysis of social cognition in amyotrophic lateral sclerosis. Cortex 88:1–7. doi:10.1016/j.cortex.2016.11.012

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank patients and their relatives, together with the other volunteers who participated to this research. The presented work was partly funded by the “eBrain: BCI and ET for ALS” Lombardy Region project.

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Correspondence to Barbara Poletti.

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On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical standard

The study has been approved by our Institute ethic committee and has, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

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Video presenting the RCPM adaptation (MOV 11,036 kb)

Video presenting the RME adaptation (MOV 12369 kb)

Diagnostic parameters for the standard and ET-based tests’ variables (PDF 106 kb)

Diagnostic parameters for ET-based VF tests (PDF 166 kb)

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Poletti, B., Carelli, L., Solca, F. et al. An eye-tracker controlled cognitive battery: overcoming verbal-motor limitations in ALS. J Neurol 264, 1136–1145 (2017). https://doi.org/10.1007/s00415-017-8506-z

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  • DOI: https://doi.org/10.1007/s00415-017-8506-z

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